Exercise training-induced adaptations associated with increases in skeletal muscle glycogen content

FEBS Journal

Volumn 280, Issue 3, 2013, Pages 916-926

  Manabe, Yasuko ^a   Gollisch, Katja S C ^a   Holton, Laura ^a   Kim, Young Bum ^b   Brandauer, Josef ^a   Fujii, Nobuharu L ^a   Hirshman, Michael F ^a   Goodyear, Laurie J ^a  

^a JOSLIN DIABETES CENTER   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

exercise; glycogen synthase; glycogen synthase kinase 3 (GSK 3); rat; skeletal muscle

Indexed keywords

GLUCOSE TRANSPORTER 4; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; INSULIN; PHOSPHOPROTEIN PHOSPHATASE 1;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE; FEMALE; GLUCOSE TRANSPORT; GLYCOGEN MUSCLE LEVEL; INSULIN SENSITIVITY; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SKELETAL MUSCLE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; IMMUNOBLOTTING; INSULIN; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; PROTEIN PHOSPHATASE 1; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

RATTUS;

EID: 84873165956     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12085     Document Type: Article

References (44)

1. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, Inzucchi S, Dresner A, Rothman DL, &, Shulman GI, (1999) Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 341, 240-246.
2. Putman CT, Jones NL, Hultman E, Hollidge-Horvat MG, Bonen A, McConachie DR, &, Heigenhauser GJ, (1998) Effects of short-term submaximal training in humans on muscle metabolism in exercise. Am J Physiol 275, E132-E139.
3. Kubo K, &, Foley JE, (1986) Rate-limiting steps for insulin-mediated glucose uptake into perfused rat hindlimb. Am J Physiol 250, E100-E102.
4. Fisher JS, Nolte LA, Kawanaka K, Han DH, Jones TE, &, Holloszy JO, (2002) Glucose transport rate and glycogen synthase activity both limit skeletal muscle glycogen accumulation. Am J Physiol Endocrinol Metab 282, E1214-E1221.
5. Goodyear LJ, &, Kahn BB, (1998) Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49, 235-261.
6. Fueger PT, Shearer J, Bracy DP, Posey KA, Pencek RR, McGuinness OP, &, Wasserman DH, (2005) Control of muscle glucose uptake: test of the rate-limiting step paradigm in conscious, unrestrained mice. J Physiol 562, 925-935.
7. Baldwin KM, Winder WW, Terjung RL, &, Holloszy JO, (1973) Glycolytic enzymes in different types of skeletal muscle: adaptation to exercise. Am J Physiol 225, 962-966.
8. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, &, Goodyear LJ, (2007) Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56, 2062-2069.
9. Franch J, Aslesen R, &, Jensen J, (1999) Regulation of glycogen synthesis in rat skeletal muscle after glycogen-depleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase. Biochem J 344 Pt 1, 231-235.
10. Tang PM, Bondor JA, Swiderek KM, &, DePaoli-Roach AA, (1991) Molecular cloning and expression of the regulatory (RG1) subunit of the glycogen-associated protein phosphatase. J Biol Chem 266, 15782-15789.
11. Armstrong CG, Browne GJ, Cohen P, &, Cohen PT, (1997) PPP1R6, a novel member of the family of glycogen-targetting subunits of protein phosphatase 1. FEBS Lett 418, 210-214.
12. Armstrong CG, Doherty MJ, &, Cohen PT, (1998) Identification of the separate domains in the hepatic glycogen-targeting subunit of protein phosphatase 1 that interact with phosphorylase A, glycogen and protein phosphatase 1. Biochem J 336 (Pt 3), 699-704.
13. Munro S, Ceulemans H, Bollen M, Diplexcito J, &, Cohen PT, (2005) A novel glycogen-targeting subunit of protein phosphatase 1 that is regulated by insulin and shows differential tissue distribution in humans and rodents. FEBS J 272, 1478-1489.
14. Cross DA, Alessi DR, Cohen P, Andjelkovich M, &, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
15. Lawrence JC Jr, &, Roach PJ, (1997) New insights into the role and mechanism of glycogen synthase activation by insulin. Diabetes 46, 541-547.
16. Durante PE, Mustard KJ, Park SH, Winder WW, &, Hardie DG, (2002) Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles. Am J Physiol Endocrinol Metab 283, E178-E186.
17. Konhilas JP, Widegren U, Allen DL, Paul AC, Cleary A, &, Leinwand LA, (2005) Loaded wheel running and muscle adaptation in the mouse. Am J Physiol Heart Circ Physiol 289, H455-H465.
18. Hickner RC, Fisher JS, Hansen PA, Racette SB, Mier CM, Turner MJ, &, Holloszy JO, (1997) Muscle glycogen accumulation after endurance exercise in trained and untrained individuals. J Appl Physiol 83, 897-903.
19. Bak JF, Jacobsen UK, Jorgensen FS, &, Pedersen O, (1989) Insulin receptor function and glycogen synthase activity in skeletal muscle biopsies from patients with insulin-dependent diabetes mellitus: effects of physical training. J Clin Endocrinol Metab 69, 158-164.
20. Mikines KJ, Sonne B, Farrell PA, Tronier B, &, Galbo H, (1989) Effect of training on the dose-response relationship for insulin action in men. J Appl Physiol 66, 695-703.
21. Goodyear LJ, Hirshman MF, Horton ED, Knutson SM, Wardzala LJ, &, Horton ES, (1991) Exercise training normalizes glucose metabolism in a rat model of impaired glucose tolerance. Metab, Clin Exp 40, 455-464.
22. Henriksen EJ, Bourey RE, Rodnick KJ, Koranyi L, Permutt MA, &, Holloszy JO, (1990) Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Physiol 259, E593-E598.
23. Matsumoto A, Nagatomo F, Mori A, Ohira Y, &, Ishihara A, (2007) Cell size and oxidative enzyme activity of rat biceps brachii and triceps brachii muscles. J Physiol Sci 57, 311-316.
24. Holm G, &, Bjorntorp P, (1980) Metabolic effects of physical training. Acta Paediatr Scand Suppl 283, 9-14.
25. Mondon CE, Dolkas CB, &, Reaven GM, (1980) Site of enhanced insulin sensitivity in exercise-trained rats at rest. Am J Physiol 239, E169-E177.
26. Wanson JC, &, Drochmans P, (1968) Rabbit skeletal muscle glycogen. A morphological and biochemical study of glycogen beta-particles isolated by the precipitation-centrifugation method. J Cell Biol 38, 130-150.
27. Meyer F, Heilmeyer LM Jr, Haschke RH, &, Fischer EH, (1970) Control of phosphorylase activity in a muscle glycogen particle. I. Isolation and characterization of the protein-glycogen complex. J Biol Chem 245, 6642-6648.
28. Printen JA, Brady MJ, &, Saltiel AR, (1997) PTG, a protein phosphatase 1-binding protein with a role in glycogen metabolism. Science 275, 1475-1478.
29. Aschenbach WG, Suzuki Y, Breeden K, Prats C, Hirshman MF, Dufresne SD, Sakamoto K, Vilardo PG, Steele M, Kim JH, et al,. (2001) The muscle-specific protein phosphatase PP1G/R(GL)(G(M)) is essential for activation of glycogen synthase by exercise. J Biol Chem 276, 39959-39967.
30. Ceulemans H, &, Bollen M, (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol Rev 84, 1-39.
31. Nielsen JN, &, Richter EA, (2003) Regulation of glycogen synthase in skeletal muscle during exercise. Acta Physiol Scand 178, 309-319.
32. Markuns JF, Wojtaszewski JF, &, Goodyear LJ, (1999) Insulin and exercise decrease glycogen synthase kinase-3 activity by different mechanisms in rat skeletal muscle. J Biol Chem 274, 24896-24900.
33. Sakamoto K, Arnolds DE, Ekberg I, Thorell A, &, Goodyear LJ, (2004) Exercise regulates Akt and glycogen synthase kinase-3 activities in human skeletal muscle. Biochem Biophys Res Commun 319, 419-425.
34. Wojtaszewski JF, Nielsen P, Kiens B, &, Richter EA, (2001) Regulation of glycogen synthase kinase-3 in human skeletal muscle: effects of food intake and bicycle exercise. Diabetes 50, 265-269.
35. Bouskila M, Hirshman MF, Jensen J, Goodyear LJ, &, Sakamoto K, (2008) Insulin promotes glycogen synthesis in the absence of GSK3 phosphorylation in skeletal muscle. Am J Physiol Endocrinol Metab 294, E28-E35.
36. Bouskila M, Hunter RW, Ibrahim AF, Delattre L, Peggie M, van Diepen JA, Voshol PJ, Jensen J, &, Sakamoto K, (2010) Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab 12, 456-466.
37. Hunter RW, Treebak JT, Wojtaszewski JF, &, Sakamoto K, (2011) Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 60, 766-774.
38. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, &, Goodyear LJ, (1998) Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47, 1369-1373.
39. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
40. Cohen P, Alemany S, Hemmings BA, Resink TJ, Stralfors P, &, Tung HY, (1988) Protein phosphatase-1 and protein phosphatase-2A from rabbit skeletal muscle. Methods Enzymol 159, 390-408.
41. Brady MJ, Nairn AC, &, Saltiel AR, (1997) The regulation of glycogen synthase by protein phosphatase 1 in 3T3-L1 adipocytes. Evidence for a potential role for DARPP-32 in insulin action. J Biol Chem 272, 29698-29703.
42. Darrow RA, &, Colowick SP, (1962) Hexokinase from baker's yeast. In Methods of Enzymology, Vol. 5, (, Colowick SP, &, Kaplan NO, eds), pp. 226-235. Academic Press, New York, NY.
43. Thomas JA, Schlender KK, &, Larner J, (1968) A rapid filter paper assay for UDPglucose-glycogen glucosyltransferase, including an improved biosynthesis of UDP-14C-glucose. Anal Biochem 25, 486-499.
44. Gilboe DP, Larson KL, &, Nuttall FQ, (1972) Radioactive method for the assay of glycogen phosphorylases. Anal Biochem 47, 20-27.